Functional outcomes of pancreaticoduodenoctomy

At present, pancreaticoduodenoctomy causes the high incidence of complications. However, it is associated with an acceptable level of postoperative mortality. With this regard and taking into consideration a significant increase in survival in pancreatic cancer, it is highly relevant to study the negative functional outcomes of surgery and develop methods for their surgical prevention. The bibliographic review focuses on the features of three main postsurgical syndromes: gastric stasis, pancreatic exocrine and endocrine insufficiency. The study shows the dependence of these syndromes on pathomorphological characteristics of pancreatic stump, preservation of the pyloric, the variant of pancreatodigestive anastomosis and other features of reconstructive stage of the surgery.

1. Kotelnikov A.G., Patutko Yu.I., Tryakin A.A. Zlokachestvennie opukholi podzeluchnoi zhelezi. V kn. Onkolologia. Klinicheskie rekomendacii / pod red. M.I. Davidova. – M.: Izdatelskaya gruppa RONC, 2015. – 680 s. (In Russ.)

2. Narayanan S., Martin A.N., Turrentine F.E. et al. Mortality after pancreaticoduodenectomy: assessing early and late causes of patient death. J. Surg. Res. 2018; 231: 304 – 308 DOI: 10.1016/j.jss.2018.05.075

3. Kawaida H., Kono H., Hosomura N. et al. Surgical techniques and postoperative pancreatic fistula after pancreatic surgery. World Journal of Gastroenterology, 2019; 25 (28): 3722 – 3737. DOI: 10.3748/wjg.v25.i28.3722

4. Conroy T., Hammel P., Hebbar M. et al. FOLFIRINOX or Gemcitabine as Adjuvant Therapy for Pancreatic Cancer. The New England Journal of Medicine. 2018, vol. 379, No 25, 2395 – 2406 DOI: 10.1056/NEJMoa1809775

5. Janssen Q.P., van Dam J.L., Doppenberg D. et al. FOLFIRINOX as initial treatment for localized pancreatic adenocarcinoma: a retrospective analysis by the Trans-Antlantic pancreatic surgery Consortium. JNCI J Natl Cancer Inst (2022) 00(0): djac 018, 1 – 9 DOI:10.1093/jnci/djac018

6. Matsunaga H., Tanaka M., Takahata S. et al. Manometric evidence of improved early gastric stasis by erythromycin after pylorus-preserving pancreatoduodenectomy. World J. Surg. 2000; 24: 1236 – 1241 doi: 10.1007/s002680010244

7. Jang J.Y., Kim S.W., Han J.K. et al. Randomized prospective trial of the effect of induced hypergastrinemia on the prevention of pancreatic atrophy after pancreatoduodenectomy in humans. Ann Surg. 2003; 237: 522 – 529 doi: 10.1097/01.SLA.0000059985.56982.11

8. Voskanyan S.E., Korotko G.F., Morfofunkcionalnaya organizacia podzheludochnoi zhelezi i ostryi posleoperacionniy pancreatit (ecsperimentalnie i klinicheskie aspekti). – M.: Litterra, 2017 – 528 s. (In Russ.)

9. Wu J.M., Kuo T.C., Yang C.Y. et al. Resolution of diabetes after pancreaticoduodenectomy in patients with and without pancreatic ductal cell adenocarcinoma. Ann Surg Oncol. 2013; 20: 242 – 249 doi: 10.1245/s10434-012-2577- у

10. Muscogiuri G., Mezza T., Prioletta A. et al. Removal of duodenum elicits GLP-1 secretion. Diabetes Care. 2013; 36: 1641 – 1646 doi: 10.2337/dc12-0811

11. Chang M.K., Lee J.H. Pathophysiology after pancreaticoduodenectomy. World Journal of Gastroenterology, 2015; 21 (19): 5794 – 5804 doi: 10.3748/wjg.v21.i19.5794.

12. Iiazawa Y., Kato H., Kishiwada M. et al. Long-term outcomes after pancreaticoduodenectomy using pair-watch suturing technique: different roles of pancreatic duct dilatation and remnant pancreatic volume for the development of pancreatic endocrine and exocrine dysfunction. Pancreatology, 2017; 17: 814 – 821 doi: 10.1016/j.pan.2017.06.008

13. Wente M.N., Bassi C., Dervenis C. et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery, 2007; 142: 761 – 768 doi: 10.1016/j.surg.2007.05.005.

14. Iqbal N., Lovegrove R.E., Tilney H.S. et al. A comparison of pancreaticoduodenectomy with extended pancreaticoduodenectomy: a metaanalysis of 2822 patients. Eur J Oncol., 2009; 35: 79 – 86 doi: 10.1016/j.ejso.2008.01.002

15. Matsumoto I., Shinzeki M., Asari S. et al. A prospective randomized comparison between pylorus- and subtotal stomach-preserving pancreatoduodenectomy on postoperative delayed gastric emptying occurrence and long-term nutritional status. J.Surg. Oncol. 2014; 109: 690 – 696 doi: 10.1002/jso.23566

16. Kawai M., Tani M., Hirono S. Pylorus ring resection reduces delayed gastric emptying in patients undergoing pancreatoduodenectomy: a prospective, randomized, controlled trial of pylorus-resecting versus pylorus-preserving pancreatoduodenectomy. Ann Surg 2011, 253: 495 – 501 doi: 10.1097/SLA.0b013e31820d98f1.

17. Kokhanenko N.Y., Pavelets K.V., Shiryaev Y.N., Radionov Y.V., Kashintsev A.A., Petrik S.V. Is the type of pancreatoduodenectomy important in evaluation of functional results of surgery? Fundamental research, 2015, №1б 537-541 (In Russ.)

18. Cai X., Zhang M., Liang C. et al. Delayed gastric emptying after pancreaticoduodenectomy: a propensity score-matched analysis and clinical nomogram study. BMC Surgery, 2020, 20: 1 – 9 doi: 10.1186/s12893-020-00809-5

19. Fahlbusch T., Luu A.M., Hohn P. et al. Impact of pylorus preserving on delayed gastric emptying after pancreaticoduodenectomy – analysis of 5000 patients based on the German StuDoQ/Pancreas-Registry. Gland Surg., 2022; 11 (1): 67 – 76 doi: 10.21037/gs-21-645

20. Eshuis W.J., van Eijck C.H., Gerhards M.F. et al. Antecolic versus retrocolic route of the gastroenteric anastomosis after pancreatoduodenectomy: a randomized controlled trial. Ann Surg., 2014; 259: 45 – 51 doi: 10.1097/SLA.0b013e3182a6f529.

21. Tamandl D., Sahora K., Prucker J. et al. Impact of the reconstruction method on delayed gastric emptying after pylorus-preserving pancreaticoduodenectomy: a prospective randomized study. World J Surg. 2014; 38: 465 – 475 doi: 10.1007/s00268-013-2274-4

22. Imamura N., Chijiiwa K., Ohuchida J. et al. Prospective randomized clinical trial of a change in gastric emptying and nutritional status after a pylorus-preserving pancreaticoduodenectomy: comparison between an antecolic and a vertical rertocolic duodenijejunostomy. HPB (Oxford). 2014; 16: 384 – 394 doi: 10.1111/hpb.12153

23. Gangavatiker R., Pal S., Javed A. et al. Effect of antecolic or retrocolic reconstruction of the gastro/duodenojejunostomy on delayed gastric emptying after pancreaticoduodenectomy: a randomized controlled trial. J Gastrointest Surg. 2011; 15: 843 – 852 doi: 10.1007/s11605-011-1480-3

24. Kurahara H., Shinchi H., Maemura K. et al. Delayed gastric emptying after pancreatoduodenectomy. J Surg Res. 2011; 171: e187 – e192 doi: 10.1016/j.jss.2011.08.002.

25. Chijiiwa K., Imamura N., Ohuchida J. et al. Prospective randomized controlled study of gastric emptying assessed by (13)C-acetate breath test after pylorus-preserving pancreaticoduodenectomy: comparison between antecollic and vertical retrocolicduodenojejunostomy. J Hepatobiliary Pancreat Surg. 2009; 16: 49 – 55 doi: 10.1007/s00534-008-0004-3

26. Shimoda M., Kubota K., Katoh M., Kita J. Effect of billroth II or Roux-en-Y reconstruction for the gastrojejunostomy on delated gastric emptying after pancreaticoduodenectomy: a randomized controlled study. Ann Surg. 2013; 257: 938 – 942 doi: 10.1097/SLA.0b013e31826c3f90

27. Ke S., Ding X.M., Gao J. et al. A prospective, randomized trial of Roux-en-Y reconstruction with isolated pancreatic drainage versus conventional loop reconstruction after pancreaticoduodenectomy. Surgery. 2013; vol.153, no. 6, pp. 743 – 752 doi: 10.1016/j.surg.2013.02.008

28. Tani M., Kawai M., Hirono S. et al. Randomized clinical trial of isolated Roux-en-Y versus conventional reconstruction after pancreaticoduodenectomy. Br.J.Surg. 2014; vol.101, no.9, pp. 1084 – 1091 doi: 10.1002/bjs.9544

29. Busquets J., Martin S., Fabregat J. et al. Randomized trial of two types of gastrojejunostomy after pancreatoduodenectomy and risk of delayed gastric emptying (PAUDA trial). The British Journal of Surgery, 2019, vol. 106, no.1, pp. 46 – 54 doi: 10.1002/bjs.11023.

30. Ma F., Fan Y., Zhang L. et al. Roux-en-Y and Billroth II reconstruction after pancreaticoduodenectomy: a meta-analysis of complications. Volume 2020, article ID 6131968, 10 pages doi: 10.1155/2020/6131968

31. Yang J., Wang C., Huang Q. Effect of Billroth II or Roux-en-Y reconstruction for the gastrojejunostomy after pancreaticoduodenectomy: meta-analysis of randomized controlled trials. Journal of gastrointestinal Surgery, 2015, vol. 19, no. 5, pp. 955 – 963 DOI 10.1007/s11605-015-2751-1

32. Dominguez-Munoz J.E. Pancreatic enzyme therapy for pancreatic exocrine insufficiency. Curr. Gastroenterol. Rep., 2007, 9: 116 – 122 DOI:10.1007/s11894-007-0005-4

33. Bartel M.J. et al., Pancreatic exocrine insufficiency in pancreatic cancer. A review of the literature. Dig Liver Dis., 2015, 47: 1013 – 1020 doi: 10.1016/j.dld.2015.06.015

34. Pathanki A.M., Attard J.A., Bradley E. et al. Pancreatic exocrine insufficiency after pancreaticoduodenectomy: current evidence and management. World J Gastrointest Pathophysiol., 2020; 11(2): 20 – 31 DOI:10.4291/wjgp.v11.i2.20

35. Roberts K.J., Bannister C.A., Schrem H. Enzyme replacement improves survival among patients with pancreatic cancer: results of a population based study. Pancreatology, 2019; 19: 114 – 121 doi: 10.1016/j.pan.2018.10.010

36. Thogari K., Tewari M., Shukla S.K. et al. Assessment of exocrine function of Pancreas following pancreaticoduodenectomy. Indian Journal of Surgical Oncology, 2019, 10 (2): 258 – 267 DOI:10.1007/s13193-019-00901-0

37. Lim P-W., Dinh K.H., Sullivan M. et al. Thirty-day outcomes underestimate endocrine and exocrine insufficiency after pancreatic resection. HPB, 2016, 18: 360 – 366 doi: 10.1016/j.hpb.2015.11.003

38. Singh V.K., Haupt M.E., Geller D.E. et al. Less common etiologies of exocrine pancreatic insufficiency. World J.Gastroenterol., 2017, 23: 7059 – 7076 doi: 10.3748/wjg.v23.i39.7059

39. Domiguez-Munoz J.E., Alvarez-Castreo A., Larino-Noia J. et al. Endoscopic ultrasonography of the pancreas as an iderect method to predict pancreatic exocrine insufficiency in patients with chronic pancreatitis. Pancreas, 2012; 41: 724 – 728 doi: 10.1097/МПА.0b013e31823b5978

40. Matsumoto J., Traverso L.W. Exocrine function following the Whipple operation as assessed by stool elastase. J. Gastrointest Surg., 2006, 10: 1225 – 1229 doi: 10.1016/дж.гассур.2006.08.001

41. Nakamura H., Murakami Y., Uemura K. Reduced pancreatic parenchymal thickness indicates exocrine pancreatic insufficiency after pancreatoduodenectomy. J.Surg.Res., 2011, 171: 473 – 478 doi: 10.1016/j.jss.2010.03.052

42. Kwak B.J., Choi H.J., You Y.K. et al. Comparative long-term outcomes for pancreatic volume change, nutritional status, and incidence of new-onset diabetes between pancreatogastrostomy and pancreatojejunostomy after pancreaticoduodenectomy. HepatoBiliary Surg Nutr., 2020; 9 (3): 284 – 295 doi: 10.21037/hbsn.2019.04.18

43. Patutko Yu.I., Kotelnikov A.G. Khirurgia raka organov biliopancreatoduodenalnoi zoni. M.: OAO “Izdatelstvo “Medicina”, 2007, 448 s. (In Russ.)

44. Halloran C.M., Cox T.F., Chauhan S. et al. Partial pancreatic resection for pancreatic malignancy is associated with sustained pancreatic exocrine failure and reduced quality of life: a prospective study. Pancreatology, 2011; 11: 535 – 545 doi: 10.1159/000333308

45. Lemaire E., O'Toole D., Sauvanet A. et al. Functional and morphological changes in the pancreatic remnant following pancreaticoduodenectomy with pancreaticogastric anastomosis. Br.J.Surg., 2000, 87: 434 – 438 doi: 10.1046/j.1365-2168.2000.01388.x

46. Sikkens E.C.M. et al. Prospective assessment of the influence of pancreatic cancer resection on exocrine pancreatic function. B.J.S., 2014, 101: 109 – 113 doi: 10.1002/bjs.9342

47. Lyubimova N.V., Kosyrev V.Y., Patyutko Y.I., Kushlinskii N.E. Analysis of elastase 1 for evaluation of excretory function of the pancreas after gastropancreatoduodenal resection. Bull Exp Biol Med., 2003, 135: 34 – 36 doi: 10.1023/a: 1023433509956

48. Beger H.G., Poch B., Mayer B., Siech M. New onset of diabetes and pancreatic exocrine insufficiency after pancreaticoduodenectomy for benign and malignant tumors. Ann Surg., 2017, 20: 1 – 16 doi: 10.1097/SLA.0000000000002422

49. Morera-ocon F.J. et al. Considerations on pancreatic exocrine function after pancreaticoduodenectomy. World J.Gastrointest. Oncol., 2014, 6: 325 – 329 doi: 10.4251/wjgo.v6.i9.325

50. Rault A., SaCunha A., Klopfenstein D. et al. Pancreaticojejunal anastomosis is preferable to pancreaticogastrostomy after pancreaticoduodenectomy for longterm outcomes of pancreatic exocrine function. J.Am.Coll Surg, 2005; 201: 239 – 244 doi: 10.1016/j.jamcollsurg.2005.03.026

51. Roeyen G., Jansen M., Ruyssinck L. et al. Pancreatic exocrine insufficiency after pancreaticoduodenectomy is more prevalent with pancreaticogastrostomy than with pancreaticojejunostomy. A retrospective multicenter observational cohort study. HPB (Oxford), 2016; 18: 1017 – 1022 doi: 10.1016/j.hpb.2016.09.002

52. Tseng D.S.J., Molenaar I.Q., Besselink M.G. et al. Pancreatic exocrine insufficiency in patients with pancreatic or periampullary cancer. Pancreas, 2016, v.45, N 3, p. 325 – 330 DOI:10.1097/МПА.0000000000000473

53. Hirata K., Nakata B., Amano R. et al. Predictive factors for change of diabetes mellitus status after pancreatectomy in preoperative diabetic and nondiabetic patients. J. Gastrointest Surg, 2014; 18: 1597 – 1603 doi: 10.1007/s11605-014-2521-5

54. Fujino Y., Suzuki Y., Matsumoto I. et al. Long-term assessment after pancreaticoduodenectomy with pancreatic duct invagination anastomosis. Surg Today., 2007; 37: 860 – 866 doi: 10.1007/s00595-007-3507-7

55. Lozinska L., Westrӧm B., Prykhodko O. et al. Decreased insulin secretion and glucose clearance in exocrine pancreas-insufficient pigs. Exp Physiol., 101.1 (2016), pp. 100 – 112 doi: 10.1113/EP085431